Environmental changes in oxygen tension reveal ROS-dependent neurogenesis and regeneration in the adult newt brain

  1. L Shahul Hameed
  2. Daniel A Berg
  3. Laure Belnoue
  4. Lasse D Jensen
  5. Yihai Cao
  6. András Simon  Is a corresponding author
  1. Karolinska Institute, Sweden
  2. Johns Hopkins University, United States
  3. Karolinska Institutet, Sweden

Abstract

Organisms need to adapt to the ecological constraints in their habitat. How specific processes reflect such adaptations are difficult to model experimentally. We tested whether environmental shifts in oxygen tension lead to events in the adult newt brain that share features with processes occuring during neuronal regeneration under normoxia. By experimental simulation of varying oxygen concentrations we show that hypoxia followed by re-oxygenation lead to neuronal death and hallmarks of an injury response, including activation of neural stem cells ultimately leading to neurogenesis. Neural stem cells accumulate reactive oxygen species (ROS) during re-oxygenation and inhibition of ROS biosynthesis counteracts their proliferation as well as neurogenesis. Importantly, regeneration of dopamine neurons under normoxia also depends on ROS-production. These data demonstrate a role for ROS-production in neurogenesis in newts, and suggest that this role may have been recruited to the capacity to replace lost neurons in the brain of an adult vertebrate.

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Author details

  1. L Shahul Hameed

    Department of Cell and Molecular Biology, Karolinska Institute, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  2. Daniel A Berg

    School of Medicine, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Laure Belnoue

    Department of Cell and Molecular Biology, Karolinska Institute, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  4. Lasse D Jensen

    Department of Microbiology and Tumor Biology, Karolinska Institute, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  5. Yihai Cao

    Department of Microbiology and Tumor Biology, Karolinska Institute, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  6. András Simon

    Department of Cell and Molecular Biology, Karolinska Institutet, Stockholm, Sweden
    For correspondence
    Andras.Simon@ki.se
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: The protocols were performed in accordance with EU regulations and were approved by local ethics committee (Permission number N429/12).

Copyright

© 2015, Hameed et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. L Shahul Hameed
  2. Daniel A Berg
  3. Laure Belnoue
  4. Lasse D Jensen
  5. Yihai Cao
  6. András Simon
(2015)
Environmental changes in oxygen tension reveal ROS-dependent neurogenesis and regeneration in the adult newt brain
eLife 4:e08422.
https://doi.org/10.7554/eLife.08422

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https://doi.org/10.7554/eLife.08422